Abstract.

Background: Literature con-

cerning lung ultrasonography is largely growing
and opening new diagnostic opportunities. The
clinical value of the ultrasonographic interstitio-
alveolar syndrome, based on artifactual (lung
comets or B-lines) rather than real images, in
the detection of lung contusion, pneumonia and
pulmonary edema, is clearly demonstrated. As
clinical echographists, though, we are living the
paradox of relying our experience in lung
pathology on images whose biophysical and ge-
netic nature is not fully understood.
Objective and Perspectives: A detailed re-
view of the ultimate findings with an analysis of
recent and past literature regarding the forma-
tion of ultrasonographic artifacts was undertak-
en with the aim of clarifying what we know and
where we are heading in this field. It is important
for us to underline how lung ultrasonography is
not morphological, as this, along with the study
of artifact formation, will be the base for the de-
velopment of a novel view able to take us from
artifact to reality in terms of quantification of
lung disease and damage.
Conclusions: Lung ultrasonographic artifacts
need to be read in a new light which will privilege
biophysical knowledge and research. In this field
a gap of basic knowledge clearly exists. A greater
understanding of the formation of acoustic arti-
facts from ultrasound interference on discretely
aerated tissues of variable density, would place
the practice of lung ultrasonography in the cor-
rect technological and clinical position.
Key Words:
Ultrasound, Sonography, Artifacts, Lung, Diagnosis.
Introduction
Study of the lung through ultrasound (US) is a
relatively recent acquisition
1
. In the last few
years, the use of lung US has received growing
attention in clinical research in intensive care pa-
European Review for Medical and Pharmacological Sciences
Lung and ultrasound: time to reflect
G. SOLDATI
1
, S. SHER
2
, A. TESTA
3
1
Emergency Department, Valle del Serchio General Hospital, Lucca (Italy)
2
Pediatric Intensive Care Unit, IRCCS Foundation, CaGranda Hospital, Milan (Italy)
3
Emergency Department, Policlinico Abano Terme, Padova (Italy)
Corresponding Author: Gino Soldati, MD; e-mail: soldatigino@yahoo.it
223
tients and trauma settings, in patients with heart
failure, adult respiratory distress syndrome,
pneumonia and pneumothorax
2-5
. More precisely,
what is recent, is the study of the partially aerat-
ed lung, as both the chest wall and the pathologic
pleural cavity have received attention ever since
echography began to be used as a diagnostic tool.
Although steps ahead have been made, we pay
today a cultural debt towards an organ which has
always been considered hostile to US
6
.
This concept has important biophysical impli-
cations as air is a barrier to the progression of ul-
trasound. An air collection larger than the ultra-
sound wave lenght used for scanning will specu-
larly reflect the acoustic energy it receives and
thus impede an anatomic scan of underlying
structures. Smaller and contiguous air collections
instead, produce complex phenomenons of re-
flection generating artefactual images
7
. Different
lung diseases, collectively included in the gener-
ic term of interstitio-alveolar syndrome, are de-
scribed not anatomically but through the analysis
of these phenomenons.
Real US Lung Imaging
Normal lung, as well as pathologic lung that is
not completely collapsed, does not offer an echo-
graphic morphologic representation with usual
clinical frequencies (3.5-15 MHz). The presence
of air in the normal lung (about 80-85% of its to-
tal volume), and that in the pathologic lung up to
a density of 0.8-0.9 g/ml, constitutes an acoustic
barrier which is inidoneous to the formation of a
morphologic echostructure
7
. The normal pleura
acts as an almost complete specular reflector
(about 85% of incident acoustic energy does not
penetrate the pleural plane). Due to the high
acoustic impedance of an elevated air to soft tis-
sue gradient, US energy cannot penetrate lung tis-
sue and it is sent back to the tranducer producing
horizontal reverberation phenomena (Figure 1)
2011; 15: 223-227
Figure 1. Normal lung sonographic appearance (10 MHz
linear probe). Pleural surface acts as a specular reflector
inducing transversal deep reverberations (thin arrows).
Figure 2. Multiple comet tails (B-Lines) arising from
the pleural line in a case of acute pulmonary edema (5 MHz
convex probe).
seen each time one tries to explore an air collec-
tion whether in the pleural cavity, in the ab-
domen or in a phantom
8,9
. Table I summarizes
examples of impedent interfaces pertinent to
lung sonography.
Morphologic lung ultrasonography is, there-
fore, a real echography of defined acoustic enti-
ties, as a critical lung mass (with a density close
to that of water), pleural thickenings or a pleural
effusion. The possibility of seeing these entities
through echography is part of radiologists,
pneumologists and emergency medicine physi-
cians culture and they have long been able to
study the thoracic wall, the pleural cavity, pneu-
monias, superficial lung tumors as well as parts
of the mediastinum
10,11
. Only in the last 10
years
12
has it been observed that a specific, sub-
compacting lung pathology is able to generate
US images which do not actually represent real
structures but artifacts (Figure 2).
Artefactual US Lung Imaging
Most of new diagnostic opportunities in the in-
terstitial pathology of the lung (extravascular
lung water expansion, edema, interstitial inflam-
mation, interstitial fibrosis) are based on sono-
graphic visual artifacts. An artifact is defined as
an erroneous interpretation of a signal by the ma-
chine. Artifacts are produced in echography
when the machine creates acoustic interference
signals as images which are not correlated to a
real morphologic entity
13
. An interesting family
of these artifacts is formed by so called ring
down artifacts, also known as lung comets or
B-lines (Figure 2). These are defined, in lung
US, as linear vertical signals that emerge from
the pleural line and extend through the entire
lung field
12,14,15
. Although well known to all those
who use and study lung US in cases of interstitial
pathology, their characterization in terms of
acoustic interactions has not been fully de-
scribed. To date, no scientific evidence exists re-
garding their genesis and whether they are simi-
lar in different types of lung pathology, or if in-
stead they may be discerned in terms of number,
density, homogeneity, spared areas and so on.
Although their presence in actual US lung im-
ages is inequivocably evident, their biophysical
G. Soldati, S. Sher, A. Testa
224
Reflection
Interfacies coefficients*
Fat/muscle 0,13
Muscle/atelectatic lung -0.01
Muscle/consolidated lung (pneumonia) -0.61
Muscle/deflated lung -0.72
Muscle/inflated lung -0.88
Muscle/air -0.99
Water/air -0.99
Table I. Reflective properties of acoustic discontinuities in
human chest
18,21
.
*Acoustic energy reflected back from anatomic interfa-
cies (1 = maximal reflection, 0 = maximal acoustic per-
meability).
Lung and ultrasound: time to reflect
225
reflect on this thesis and comprehend the real and
complex nature of ultrasound lung artifacts.
Moreover, in order to see and acquire these in-
terference phenomena, we are using machines
that paradoxically consider them as errors and
that technology is working to adjust. We are
studying phenomena that appear to those who
design and build echographic machines as para-
sites on which to carry out a sort of electronic
cosmesis
21
.
What occurs is not a purely theoretical or tech-
nical problem, it would be so if these effects
were only encountered in the laboratory, but ac-
tually several clinical studies are based on data
regarding pathologic lungs that appear as non-
structured fields of B-lines
12,22-25
. And how can
we deny the value of being able to use these im-
ages clinically, for the detection and differentia-
tion of lung disease? How can we deplore the
formulation of the echographic interstitial syn-
drome based on the presence of few to coalescent
B-lines
12,22
? No doubt exists regarding the value
of the echographic interstitial syndrome in the
detection of lung pathology, what is missing is a
thorough understanding of the formation of US
artifacts both in terms of biophysical phenomena
but especially of anatomic and structural lung al-
terations.
The interstitial, or interstitio-alveolar syn-
drome, is an anatomo-pathological entity but, un-
like the alveolar syndrome which has its respec-
tive echographic anatomy (a lung consolidation),
it creates artifacts instead of real images. Evi-
dence shows that what is tagged as echographic
interstitial syndrome does not topographically go
characterization is not so clear at all. We are in
the paradoxical situation of being able to under-
stand certain subatomic interactions and at the
same time not know what simple acoustic inter-
actions as B-lines or the white lung stand for
7
.
The few Authors who have intended to study
the formation of these artifacts on biologic and
non-biologic substrates have been able to classify
US artifacts as reverberation and/or resonance
phenomena based on limited past scientific evi-
dence
7,14
. In fact, historically, the only study ad-
dressing these artifacts formation was the one
carried out by Avruch et al.
14
on the concept of
US induced resonance between small air bubbles
arranged in tetrahedrons
7
. Although this study
leaves several perplexities as a pure in vivo phe-
nomenon, numerous subsequent ones refer to
Avruchs resonant tetrahedrons as the paradigm
of a diffuse acoustic phenomenon described
prevalently, but confusedly, as ring down arti-
facts
14,16,17
.
As often happens in science, we may find with
surprise that several decades ago certain physi-
cists, and not physicians, had described the
acoustic behavior of the lung, not in terms of im-
ages but of acoustic interactions and permeability,
first admitting and later denying productive inter-
ference as all that goes beyond acoustic reverber-
ations on multiple and discrete air collections
18
.
What seems to emerge is that lung tissue per-
meability to US is correlated to its density or its
porosity, in other words to its increase in weight
or, furthermore, to its loss of air content or defla-
tion (deflated lung with same weight, isobaric,
with no intrinsic pathology)
19
. In this context, the
B-lines in their variable arrangements (but are
they really all arrangements of different B-lines?)
appear to the machine as signals that indicate a
physical event corresponding to a physiopatho-
logic lung alteration
20
. And if it is so, the image
we create through echography is actually redun-
dant and a simple display showing numbers, per-
haps a color map, or Cartesian axes as the results
of complex equations and algorithms solved,
could be enough for diagnostic purposes.
The Interstitio-Alveolar Syndrome
Sonographic interstitio-alveolar syndrome was
first described in 1997
12
. To date, the vast majori-
ty of Authors refer to the classical Lichtensteins
interpretation. This vision emphasizes the role of
subpleural interlobular septa for the genesis of
lung comets (B-Lines). We believe it is time to
Figure 3. Synthetic comet tails arising from a 10 10 7
mm porous wet polyurethane scaffold insonated with a 6,6
MHz linear probe.
226
beyond the first two millimeters of subpleural
lung tissue, although what is seen inequivocally
fills the entire display.
In this view, we are building whole chapters of
echographic imaging regarding different lung en-
tities, based on signs we do not fully know and
which are characterized by an intrinsic elusive-
ness. This uncertainty derives from the fact that
these vertical artifacts, contrary to current opin-
ion, do not appear to correlate with a specific
anatomical structure. A recent work on this topic
7
and rare preexisting studies
14,16
have demonstrat-
ed how similar artifacts may be created in proper
bubble systems both in vitro and in vivo. There is
evidence that analogous signals are produced in
jelly systems, in foam systems or on a
polyurethane scaffold (Figure 3) (personal un-
published data) independent of a tetrahedric or
definite anatomic structure (as interlobular lung
septa)
7,12,26
. It appears ever clearer how signals
analogous to B-lines are seen each time the in-
sonated substrate increases its permeability to US
due to geometric alterations in its porosity (i.e.
density).
Perspectives and Conclusions
Lung sonography is an interesting diagnostic
method, with a high sensitivity in cases of inter-
stitial lung pathology, in particular located in
near subpleural parenchyma
2,3,12,23,24,26
. However,
we believe that lung US artifacts need to be read
in a new perspective which will privilege bio-
physical research and clarify how this type of
echography is not morphological. Although we
have demonstrated the link between echographic
syndromes and certain lung pathology it does not
mean we should still be talking, in these specific
cases, of echography.
It may seem provocative but if we believe in
lung US we should at this point plan a future that
considers the relationship between artifactual
lung images and lung density. Density will be
isobaric when what varies is air extension and
relatively isovolumetric when what varies is the
interstitial space (or organ weight).
Will it be a radiant future? No data yet allows
us to affirm this. If we think, though, about the
applications of Computerized Tomography
27,28
in
the quantitative evaluation of subpleural lung
density and to the clinical implications this had
in terms of pulmonary edema, acute lung injury
and adult respiratory distress syndrome, even if
the close ideal of lung echography was only a
discrete, strictly cortical, densitometric model,
we could consider ourselves satisfied.
References
1) SOLDATI G, SHER S. Bedside lung ultrasound in criti-
cal care practice. Minerva Anestesiol 2009; 75:
509-517.
2) PICANO E, GARGANI L, GHEORGHIADE M. Why, when,
and how to assess pulmonary congestion in heart
failure: pathophysiological, clinical, and method-
ological implications. Heart Fail Rev 2010; 15: 63-
72.
3) COPETTI R, SOLDATI G, COPETTI P. Chest sonography:
A useful tool to differentiate acute cardiogenic
pulmonary edema from acute respiratory distress
syndrome. Cardiovasc Ultrasound 2008; 6: 16.
4) PARLAMENTO S, COPETTI R, DI BARTOLOMEO S. Evalua-
tion of lung ultrasound for the diagnosis of pneu-
monia in the ED. Am J Emerg Med 2009; 27:
379-384.
5) SOLDATI G, TESTA A, SHER S, PIGNATARO G, LA SALA M,
GENTILONI SILVERI N. Occult traumatic pneumotho-
rax: diagnostic accuracy of lung ultrasonography
in the emergency department. Chest 2008; 133:
204-211.
6) DRAZEN JM, WEINBERGER SA. APPROACH TO THE PATIENT
WITH DISEASE OF RESPIRATORY SYSTEM. IN: KASPER DL, FAUCI
AS, LONGO DL, BRAUNWALD E, HAUSER SL, JAMESON JL
(EDS). Harrisons principles of internal medicine.
16th ed. New York, Mc Graw Hill, 2005: p. 1506.
7) SOLDATI G, COPETTI R, SHER S. Sonographic intersti-
tial syndrome: The sound of lung water. J Ultra-
sound Med 2009; 28: 163-174.
8) KREMKAU FW, TAYLOR KJW. Artifacts in ultrasound
imaging. J Ultrasound Med 1986; 5: 227-237.
9) SOLDATI G. Sonographic findings in pulmonary dis-
eases. Radiol Med 2006; 111: 507-515.
10) MATHIS G. Thorax sonography - Part I: Chest wall
and pleura. Ultrasound Med Biol 1997; 23: 1131-
1139.
11) MATHIS G. Thorax sonography - Part II: Peripheral
pulmonary consolidations. Ultrasound Med Biol
1997; 23: 1141-1153.
12) LICHTENSTEIN D, MEZIRE G, BIDERMAN P, GEPNER A,
BARR O. The comet-tail artifact: An ultrasound
sign of alveolar-interstitial syndrome. Am J Respir
Crit Care Med 1997; 156: 1640-1646.
13) SKOLNICK ML, MEIRE HB, LECKY JW. Common arti-
facts in ultrasound scanning. J Clin Ultrasound
1975; 3: 273-280.
G. Soldati, S. Sher, A. Testa
14) AVRUCH L, COOPERBERG PL. The ring down artifact. J
Ultrasound Med 1985; 4: 8-14.
15) KOHZAKI S, TSURUSAKI K, UETANI M, NAKANISHI K,
HAYASHI K. The aurora sign: An ultrasonographic
sign suggesting parenchymal lung disease. Br J
Radiol 2003; 76: 437-443.
16) FELDMAN MK, KATYAL S, BLACKWOOD MS. US arti-
facts. Radiographics 2009; 29: 1179-1189.
17) LIM JH, LEE KS, KIM TS, CHUNG MP. Ring-down arti-
facts posterior to the right hemidiaphragm on ab-
domi nal sonography: si gn of pul monary
parenchymal abnormalities. J Ultrasound Med
1999; 18: 403-410.
18) DUNN F, FRY WJ. Ultrasonic absorption and reflection
by lung tissue. Phys Med Biol 1961; 5: 401-410.
19) DUNN F. Attenuation and speed of ultrasound in
lung. J Acoustic Soc Am 1974; 56: 1638-1639.
20) REISSIG A, KROEGEL C. Transthoracic sonography of
diffuse parenchymal lung disease. J Ultrasound
Med 2003; 22: 173-180.
21) SZABO TL. Diagnostic ultrasound imaging. Amster-
dam, Elsevier Academic Press, 2004.
22) LICHTENSTEIN D, MEZIERE G. A lung ultrasound sign
allowing bedside distinction between pulmonary
edema and COPD: the comet-tail artifact. Inten-
sive Care Med 1998; 24: 1331-1334.
23) JAMBRIK Z, MONTI S, COPPOLA V et al. Usefulness of
ultrasound lung comets as non radiologic sign of
extravascular lung water. Am J Cardiol 2004; 93:
1265-1270.
24) GARGANI L, FRASSI F, SOLDATI G, TESORIO P, GHEORGHI-
ADE M, PICANO E. Ultrasound lung cometsfor differ-
ential diagnosis of acute cardiogenic dipnoea: A
comparison with natriuretic peptides. Eur J Heart
Fail 2008; 10:70-77.
25) WILSON SR, BURNS PN, WILKINSON LM, SIMPSON DH,
MURADALI D. Gas at abdominal US: Appearance,
relevance, and analysis of artifacts. Radiology
1999; 210: 113-123.
26) FRASSI F, GARGANI L, GLIGOROVA S, CIAMPI Q, MOTTOLA
G, PICANO E. Clinical and echocardiographic de-
terminants of ultrasound lung comets. Eur J
Echocardiogr 2007; 8: 474-479.
27) GATTINONI L, CAIRONI P, CRESSONI M, CHIUMELLO D,
RANIERI VM, QUINTEL M, RUSSO S, PATRONITI N, CORNE-
JO R, BUGEDO G. Lung recruitment in patients with
the acute respiratory distress syndrome. N Engl J
Med 2006; 354: 1775-1786.
28) GATTINONI L, CAIRONI P, VALENZA F, CARLESSO E. The
role of CT-scan studies for the diagnosis and
therapy of acute respiratory distress syndrome.
Clin Chest Med 2006; 27: 559-570.
227
Lung and ultrasound: time to reflect